Flower heads in Asteraceae-recruitment of conserved developmental regulators to control the flower-like inflorescence architecture

Abstract

Inflorescences in the Asteraceae plant family, flower heads, or capitula, mimic single flowers but are highly compressed structures composed of multiple flowers. This transference of a flower-like appearance into an inflorescence level is considered as the key innovation for the rapid tribal radiation of Asteraceae. Recent molecular data indicate that Asteraceae flower heads resemble single flowers not only morphologically but also at molecular level. We summarize this data giving examples of how rewiring of conserved floral regulators have led to evolution of morphological innovations in Asteraceae. Functional diversification of the highly conserved flower meristem identity regulator LEAFY has shown a major role in the evolution of the capitulum architecture. Furthermore, gene duplication and subsequent sub- and neofunctionalization of SEPALLATA- and CYCLOIDEA-like genes in Asteraceae have been shown to contribute to meristem determinacy, as well as flower type differentiation-key traits that specify this large family. Future challenge is to integrate genomic, as well as evolutionary developmental studies in a wider selection of Asteraceae species to understand the detailed gene regulatory networks behind the elaborate inflorescence architecture, and to promote our understanding of how changes in regulatory mechanisms shape development.

References

[1] Funk, V. A., Susanna, A., Stuessy, T. F. & Bayer, R. J. Systematics, evolution, and biogeography of Compositae. (International Association for Plant Taxonomy, Vienna, 2009).

[2] Jeffrey, C. Compositae: Introduction with key to tribes. in Flowering plants: Eudicots; Asterales (eds. Kadereit, J. J. W. & Jeffrey, C. ) 61-87 (Springer-Verlag, Berlin, 2007).

[3] Barreda, V. D. et al. Eocene Patagonia fossils of the daisy family. Science 329, 1621 (2010).

[4] Barreda, V. D. et al. An extinct Eocene taxon of the daisy family (Asteraceae): evolutionary, ecological and biogeographical implications. Ann. Bot. 109, 127-134 (2012).

[5] Barker, M. S. et al. Multiple paleopolyploidizations during the evolution of the Compositae reveal parallel patterns of duplicate gene retention after millions of years. Mol. Biol. Evol. 25, 2445-2455 (2008).

[6] Barker, M. S. et al. Most Compositae (Asteraceae) are descendants of a paleohexaploid and all share a paleotetraploid ancestor with the Calyceraceae. Am. J. Bot. 103, 1203-1211 (2016).

[7] Stuessy, T. F., Spooner, D. M. & Evans, K. A. Adaptive significance of ray corollas in Helianthus grosseserratus (Compositae). Am. Midl. Nat. 115, 191-197 (1986).

[8] Sun, M. & Ganders, F. R. Outcrossing rates and allozyme variation in rayed and rayless morphs of Bidens pilosa. Heredity 64, 139-143 (1990).

[9] Andersson, S. Pollinator and nonpollinator selection on ray morphology in Leucanthemum vulgare (Oxeye daisy, Asteraceae). Am. J. Bot. 95, 1072-1078 (2008).

[10] Zhao, Y. et al. Evolutionary co-option of floral meristem identity genes for patterning of the flower-like Asteraceae inflorescence. Plant Physiol. 172, 284-296 (2016).

[11] Zhang, T. et al. Dissecting functions of SEPALLATA-like MADS box genes in patterning of the pseudanthial inflorescence of Gerbera hybrida. New Phytol. 216, 939-954 (2017).

[12] Bremer, K. Asteraceae: Cladistics and Classification. (Timber Press, Portland, OR, 1994).

[13] Harris, E. M. Inflorescence and floral ontogeny in Asteraceae: a synthesis of historical and current concepts. Bot. Rev. 61, 93-278 (1995).

[14] Claßen-Bockhoff, R. Functional units beyond the level of the capitulum and cypsela in Compositae. in Compositae: biology & utilization (eds. Cagliari, R. D. S. & Hind, D. J. N.) 129-160 (Royal Botanic Gardens, Kew, 1996).

[15] Leins, P. & Gemmeke, V. Infloreszenz- und Blutenentwicklung bei der Kugeldistel Echinops exaltatus (Asteraceae). Plant Syst. Evol. 132, 189-204 (1979).

[16] Harris, E. M. Developmental evidence for the derivation of syncephalia in Lagascea (Heliantheae; Asteraceae). Am. J. Bot. 81, 1139-1148 (1994).

[17] Bello, M. A., Cubas, P., Álvarez, I., Sanjuanbenito, G. & Fuertes-Aguilar, J. Evolution and expression patterns of CYC/TB1 genes in Anacyclus: phylogenetic insights for floral symmetry genes in Asteraceae. Front. Plant Sci. 8, 1-12 (2017).

[18] Harris, E. M., Tucker, S. C. & Urbatsch, L. E. Floral initiation and early development in Erigeron philadelphicus (Asteraceae). Am. J. Bot. 78, 108-121 (1991).

[19] Broholm, S. K., Teeri, T. H. & Elomaa, P. Molecular control of inflorescence development in Asteraceae. in Advances in Botanical Research, The molecular genetics of floral transition and flower development (eds. Jacquot, J.-P., Gadal, P. & Fornara, F.) 72, 297-333 (Academic Press, Elsevier, Oxford, 2014).

[20] McKim, S. & Hay, A. Patterning and evolution of floral structures - marking time. Curr. Opin. Genet. Dev. 20, 448-453 (2010).

[21] Moyroud, E., Kusters, E., Monniaux, M., Koes, R. & Parcy, F. LEAFY blossoms. Trends Plant. Sci. 15, 346-352 (2010).

[22] Weigel, D., Alvarez, J., Smyth, D., Yanofsky, M. & Meyerowitz, E. LEAFY controls floral meristem identity in Arabidopsis. Cell 69, 843-859 (1992).

[23] Chae, E., Tan, Q. K.-G., Hill, T. A. & Irish, V. F. An Arabidopsis F-box protein acts as a transcriptional co-factor to regulate floral development. Development 135, 1235-1245 (2008).

[24] Liu, C., Xi, W., Shen, L., Tan, C. & Yu, H. Regulation of floral patterning by flowering time genes. Dev. Cell 16, 711-722 (2009).

[25] Souer, E. et al. Patterning of inflorescences and flowers by the F-box protein DOUBLE TOP and the LEAFY homolog ABERRANT LEAF AND FLOWER of Petunia. Plant Cell 20, 2033-2048 (2008).

[26] Lippman, Z. B. et al. The making of a compound inflorescence in tomato and related nightshades. PLoS Biol. 6, 2424-2435 (2008).

[27] Cronquist, A . The Compositae revisited. Brittonia 29, 137-153 (1977).

[28] Claßen-Bockhoff, R. & Bull-Hereñu, K. Towards an ontogenetic understanding of inflorescence diversity. Ann. Bot. 112, 1523-1542 (2013).

[29] Endress, P. K. Disentangling confusions in inflorescence morphology: patterns and diversity of reproductive shoot ramification in angiosperms. J. Syst. Evol. 48, 225-239 (2010).

[30] Pozner, R., Zanotti, C. & Johnson, L. A. Evolutionary origin of the Asteraceae capitulum: insights from Calyceraceae. Am. J. Bot. 99, 1-13 (2012).

[31] Weberling, F. Morphology of flowers and inflorescences. (Cambridge University Press, Cambridge, 1992).

[32] Teeri, T. H. et al. Reproductive meristem fates. J. Exp. Bot. 57, 3445-3455 (2006).

[33] Uimari, A. et al. Integration of reproductive meristem fates by a SEPALLATA-like MADS-box gene. Proc. Natl. Acad. Sci. USA 101, 15817-15822 (2004).

[34] Zahn, L. M. et al. The evolution of the SEPALLATA subfamily of MADS-box genes: a preangiosperm origin with multiple duplications throughout angiosperm history. Genetics 169, 2209-2223 (2005).

[35] Ruokolainen, S., Ng, Y. P., Albert, V. A., Elomaa, P. & Teeri, T. H. Large scale interaction analysis predicts that the Gerbera hybrida floral E function is provided both by general and specialized proteins. BMC Plant Biol. 10, 129 (2010).

[36] Pelaz, S., Ditta, G. S., Baumann, E., Wisman, E. & Yanofsky, M. F. B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405, 200-203 (2000).

[37] Ditta, G., Pinyopich, A., Robles, P., Pelaz, S. & Yanofsky, M. F. The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Curr. Biol. 14, 1935-1940 (2004).

[38] Kotilainen, M. et al. GRCD1, an AGL2-like MADS box gene, participates in the C function during stamen development in Gerbera hybrida. Plant Cell 12, 1893-1902 (2000).

[39] Teeri, T. H., Elomaa, P., Kotilainen, M. & Albert, V. A. Mining plant diversity: Gerbera as a model system for plant developmental and biosynthetic research. Bioessays 28, 756-767 (2006).

[40] Ferrario, S., Immink, R. G. H., Shchennikova, A., Busscher-Lange, J. & Angenent, G. C. The MADS box gene FBP2 is required for SEPALLATA function in Petunia. Plant Cell 15, 914-925 (2003).

[41] Ampomah-Dwamena, C., Morris, B. A., Sutherland, P., Veit, B. & Yao, J. Down-regulation of TM29, a tomato SEPALLATA homolog, causes parthenocarpic fruit development and floral reversion. Plant Physiol. 130, 605-617 (2002).

[42] Lenhard, M., Bohnert, A., Jürgens, G. & Laux, T . Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between WUSCHEL and AGAMOUS. Cell 105, 805-814 (2001).

[43] Sun, B., Xu, Y., Ng, K. H. & Ito, T. A timing mechanism for stem cell maintenance and differentiation in the Arabidopsis floral meristem. Genes Dev. 23, 1791-1804 (2009).

[44] Liu, X. et al. AGAMOUS terminates floral stem cell maintenance in Arabidopsis by directly repressing WUSCHEL through recruitment of polycomb group proteins. Plant Cell 23, 3654-3670 (2011).

[45] Kwiatkowska, D. Flowering and apical meristem growth dynamics. J. Exp. Bot. 59, 187-201 (2008).

[46] Reddy, G. V. & Meyerowitz, E. M. Stem-cell homeostasis and growth dynamics can be uncoupled in the Arabidopsis shoot apex. Science 310, 663-667 (2005).

[47] Brand, U., Fletcher, J. C., Hobe, M., Meyerowitz, E. M. & Simon, R. Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289, 617-619 (2000).

[48] Schoof, H. et al. The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100, 635-644 (2000).

[49] Marc, J. A. N. & Palmer, J. H. Changes in mitotic activity and cell size in the apical meristem of Helianthus annuus L. during the transition to flowering. Am. J. Bot. 69, 768-775 (1982).

[50] Hileman, L. C. Trends in flower symmetry evolution revealed through phylogenetic and developmental genetic advances. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 369, 20130348 (2014).

[51] Hileman, L. C. Bilateral flower symmetry - how, when and why?. Curr. Opin. Plant Biol. 17, 146-152 (2014).

[52] Broholm, S. K. et al. A TCP domain transcription factor controls flower type specification along the radial axis of the Gerbera (Asteraceae) inflorescence. Proc. Natl. Acad. Sci. USA 105, 9117-9122 (2008).

[53] Kim, M. et al. Regulatory genes control a key morphological and ecological trait transferred between species. Science 322, 1116-1119 (2008).

[54] Chapman, M. A., Leebens-Mack, J. H. & Burke, J. M. Positive selection and expression divergence following gene duplication in the sunflower CYCLOIDEA gene family. Mol. Biol. Evol. 25, 1260-1273 (2008).

[55] Chapman, M. A. et al. Genetic analysis of floral symmetry in Van Gogh’s sunflowers reveals independent recruitment of CYCLOIDEA genes in the Asteraceae. PLoS Genet. 8, e1002628 (2012).

[56] Tähtiharju, S. et al. Evolution and diversification of the CYC/TB1 gene family in Asteraceae - a comparative study in gerbera (Mutisieae) and sunflower (Heliantheae). Mol. Biol. Evol. 29, 1155-1166 (2012).

[57] Juntheikki-Palovaara, I. et al. Functional diversification of duplicated CYC2 clade genes in regulation of inflorescence development in Gerbera hybrida (Asteraceae). Plant J. 79, 783-796 (2014).

[58] Garcês, H. M. P., Spencer, V. M. R. & Kim, M. Control of floret symmetry by RAY3, SvDIV1B, and SvRAD in the capitulum of Senecio vulgaris. Plant Physiol. 171, 2055-2068 (2016).

[59] Huang, D. et al. Identification and characterization of CYC-like genes in regulation of ray floret development in Chrysanthemum morifolium. Front. Plant Sci. 7, 1-15 (2016).

[60] Panero, J. L. & Funk, V. A. The value of sampling anomalous taxa in phylogenetic studies: major clades of the Asteraceae revealed. Mol. Phylogenet. Evol. 47, 757-782 (2008).

[61] Carlson, S. E., Howarth, D. G. & Donoghue, M. J. Diversification of CYCLOIDEA-like genes in Dipsacaceae (Dipsacales): implications for the evolution of capitulum inflorescences. BMC Evol. Biol. 11, 1-13 (2011).

[62] Claßen-Bockhoff, R., Ruonala, R., Bull-Hereñu, K., Marchant, N. & Albert, V. A. The unique pseudanthium of Actinodium (Myrtaceae) - morphological reinvestigation and possible regulation by CYCLOIDEA-like genes. EvoDevo 4, 8 (2013).

[63] Fambrini, M., Salvini, M., Basile, A. & Pugliesi, C. Transposon-dependent induction of Vincent van Gogh’s sunflowers: exceptions revealed. Genesis 52, 315-327 (2014).

[64] Fambrini, M., Salvini, M. & Pugliesi, C. A transposon-mediate inactivation of a CYCLOIDEA-like gene originates polysymmetric and androgynous ray flowers in Helianthus annuus. Genetica 139, 1521-1529 (2011).

[65] Luo, D., Carpenter, R., Vincent, C., Copsey, L. & Coen, E. Origin of floral asymmetry in Antirrhinum. Nature 383, 794-799 (1996).

[66] Luo, D. et al. Control of organ asymmetry in flowers of Antirrhinum. Cell 99, 367-376 (1999).

[67] Corley, S. B., Carpenter, R., Copsey, L. & Coen, E. Floral asymmetry involves an interplay between TCP and MYB transcription factors in. Proc. Natl. Acad. Sci. USA 102, 5068-5073 (2005).

[68] Costa, M. M. R., Fox, S., Hanna, A. I., Baxter, C. & Coen, E. Evolution of regulatory interactions controlling floral asymmetry. Development 132, 5093-5101 (2005).

[69] Yang, X. et al. Evolution of double positive autoregulatory feedback loops in CYCLOIDEA2 clade genes is associated with the origin of floral zygomorphy. Plant Cell 24, 1834-1847 (2012).

[70] Laitinen, R. A. E., Broholm, S., Albert, V. A., Teeri, T. H. & Elomaa, P. Patterns of MADS-box gene expression mark flower-type development in Gerbera hybrida (Asteraceae). BMC Plant Biol. 6, 11 (2006).

[71] Liu, H. et al. Whole-transcriptome analysis of differentially expressed genes in the vegetative buds, floral buds and buds of Chrysanthemum morifolium. PLoS ONE 10, 1-24 (2015).

[72] Reyes-Chin-Wo, S. et al. Genome assembly with in vitro proximity ligation data and whole-genome triplication in lettuce. Nat. Commun. 8, 14953 (2017).

[73] Badouin, H. et al. The sunflower genome provides insights into oil metabolism, flowering and Asterid evolution. Nature 546, 148-152 (2017).

[74] Peng, Y. et al. De novo genome assembly of the economically important weed horseweed using integrated data from multiple sequencing platforms. Plant Physiol. 166, 1241-1254 (2014).

[75] Scaglione, D. et al. The genome sequence of the outbreeding globe artichoke constructed de novo incorporating a phase-aware low-pass sequencing strategy of F1 progeny. Sci. Rep. 6, 1-17 (2016).

[76] Shen, Q. et al. The genome of Artemisia annua provides insight into the evolution of Asteraceae family and artemisinin biosynthesis. Mol. Plant (2018), in press. https://doi.org/10.1016/j.molp.2018.03.015

[77] Chanderbali, A. S., Berger, B. A., Howarth, D. G., Soltis, P. S. & Soltis, D. E. Evolving ideas on the origin and evolution of flowers: new perspectives in the genomic era. Genetics 202, 1255-1265 (2016).

[78] Berger, B. A. et al. The unexpected depths of genome-skimming data: a case study examining Goodeniaceae floral symmetry genes. Appl. Plant Sci. 5, 1700042 (2017).

[79] Berti, F., Fambrini, M., Turi, M., Bertini, D. & Pugliesi, C. Mutations of corolla symmetry affect carpel and stamen development in Helianthus annuus. Can. J. Bot. 83, 1065-1072 (2005).